Novel Zn2+ coordination by the regulatory N-terminus metal binding domain of Arabidopsis thaliana Zn2+-ATPase HMA2

Biochemistry

Volumn 46, Issue 26, 2007, Pages 7754-7764

  Eren, Elif ^a   González Guerrero, Manuel ^a   Kaufman, Brad M ^a   Argüello, José M ^a  

^a Worcester Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; HOMOLOGY; METAL BINDING DOMAIN; STRUCTURAL COMPARISON;

ADENOSINETRIPHOSPHATE; AMINO ACIDS; COORDINATION REACTIONS; DICHROISM; MUTAGENESIS; ZINC;

PLANTS (BOTANY);

ADENOSINE TRIPHOSPHATASE; ALANINE; AMINO ACID; CYSTEINE; HMA2 PROTEIN; UNCLASSIFIED DRUG; ZINC; ARABIDOPSIS PROTEIN; HMA2 PROTEIN, ARABIDOPSIS; ZN(II) TRANSLOCATING P TYPE ATPASE; ZN(II)-TRANSLOCATING P-TYPE ATPASE;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; ENZYME ACTIVITY; GENE SEQUENCE; HOMEOSTASIS; METAL BINDING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EUKARYOTA;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; ZINC;

EID: 34347336571     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7001345     Document Type: Article

References (67)

1. Argüello, J. M. (2003) Identification of ion selectivity determinants in heavy metal transport P1B-type ATPases, J. Membr. Biol. 195, 93-108.
2. Rensing, C., Ghosh, M., and Rosen, B. P. (1999) Families of soft-metal-ion transporting ATPases, J. Bacteriol. 181, 5891-5897.
3. Axelsen, K. B., and Palmgren, M. G. (1998) Evolution of substrate specificities in the P-type ATPase superfamily, J. Mol. Evol. 46, 84-101.
4. 1B-ATPases-an ancient family of transition metal pumps with diverse function in plants, Trends Plant Sci. 10, 491-502.
5. Lutsenko, S., and Petris, M. J. (2003) Function and regulation of the mammalian copper-transporting ATPases: insights from biochemical and cell biological approaches, J. Membr. Biol. 192, 1-12.
6. Bull, P. C., and Cox, D. V. (1994) Wilson disease and Menkes disease: new handles on heavy-metal transport, Trends Genet. 10, 246-252.
7. Hirayama, T., Kieber, J. J., Hirayama, N., Kogan, M., Guzman, P., Nourizadeh, S., Alonso, J. M., Dailey, W. P., Dancis, A., and Ecker, J. R. (1999) RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis, Cell 97, 383-393.
8. +2 homeostasis, Plant Physiol. 136, 3712-3723.
9. Hussain, D., Haydon, M. J., Wang, Y., Wong, E., Sherson, S. M., Young, J., Camakaris, J., Harper., J. F., and Cobbett, C. S. (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in arabidopsis, Plant Cell 16, 1327-1339.
10. Andres-Colas, N., Sancenon, V., Rodriguez-Navarro, S., Mayo, S., Thiele, D. J., Ecker, J. R., Puig, S., and Penarrubia, L. (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots, Plant J. 45, 225-236.
11. Shikanai, T., Muller-Moule, P., Munekage, Y., Niyogi, K. K., and Pilon, M. (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts, Plant Cell 15, 1333-1346.
12. Eren, E., Kennedy, D. C., Maroney, M. J., and Argüello, J. M. (2006) A novel regulatory metal binding domain is present in the C terminus of Arabidopsis Zn2+-ATPase HMA2, J. Biol. Chem. 281, 33881-33891.
13. 11 stretch, FEBS Lett. 579, 1515-1522.
14. Lutsenko, S., and Kaplan, J. H. (1995) Organization of P-type ATPases: significance of structural diversity, Biochemistry 34, 15607-15613.
15. +- transporting P1B-type ATPases, J. Biol. Chem. 279, 54802-54807.
16. Lowe, J., Vieyra, A., Catty, P., Guillain, F., Mintz, E., and Cuillel, M. (2004) A mutational study in the transmembrane domain of Ccc2p, the yeast Cu(I)-ATPase, shows different roles for each Cys-Pro-Cys cysteine, J. Biol. Chem. 279, 25986-25994.
17. Dutta, S. J., Liu, J., Hou, Z., and Mitra, B. (2006) Conserved aspartic acid 714 in transmembrane segment 8 of the ZntA subgroup of P1B-type ATPases is a metal-binding residue, Biochemistry 45, 5923-5931.
18. Wu, C.-C., Gardarin, A., Martel, A., Mintz, E., Guillain, F., and Catty, P. (2006) The cadmium transport Sites of CadA, the Cd2+-ATPase from Listeria monocytogenes, J. Biol. Chem. 281, 29533-29541.
19. Sazinsky, M. H., Mandal, A. K., Argüello, J. M., and Rosenzweig, A. C. (2006) Structure of the ATP binding domain from the Archaeoglobus fulgidus Cu+-ATPase, J. Biol. Chem. 281, 11161-11166.
20. Sazinsky, M. H., Agarwal, S., Argüello, J. M., and Rosenzweig, A. C. (2006) Structure of the actuator domain from the Archaeoglobus fulgidus Cu(+)-ATPase, Biochemistry 45, 9949-9955.
21. Arnesano, F., Banci, L., Bertini, I., Ciofi-Baffoni, S., Molteni, E., Huffman, D. L., and O'Halloran, T. V. (2002) Metallochaperones and metal-transporting ATPases: a comperative analysis of sequences and structures, Genome Res. 12, 255-271.
22. Banci, L., Bertini, I., Ciofi-Baffoni, S., Huffman, D. L., and O'Halloran, T. V. (2001) Solution structure of the yeast copper transporter domain Ccc2a in the Apo and Cu(I)-loaded States, J. Biol. Chem. 276, 8415-8426.
23. Gitschier, J., Moffat, B., Reilly, D., Wood, W. I., and Fairbrother, W. J. (1998) Solution structure of the fourth metal-binding domain from the Menkes copper-transporting ATPase, Nat. Struct. Biol. 5, 47-54.
24. Banci, L., Bertini, I., Del Conte, R., Markey, J., and Ruiz-Duenas, F. J. (2001) Copper trafficking: the solution structure of Bacillus subtilis CopZ, Biochemistry 40, 15660-15668.
25. Rosenzweig, A. C., Huffman, D. L., Hou, M. Y., Wernimont, A. K., Pufahl, R. A., and O'Halloran, T. V. (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 A resolution, Structure 7, 605-617.
26. DiDonato, M., Narindrasorasak, S., Forbes, J. R., Cox, D. W., and Sarkar, B. (1997) Expression, purification, and metal binding properties of the N-terminal domain from the Wilson disease putative copper-transporting ATPase (ATP7B), J. Biol. Chem. 272, 33279-33282.
27. Lutsenko, S., Petrukhin, K., Cooper, M. J., Gilliam, C. T., and Kaplan, J. H. (1997) N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson's and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat, J. Biol. Chem. 272, 18939-18944.
28. Huffman, D. L., and O'Halloran, T. V. (2000) Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2, J. Biol. Chem. 275, 18611-18614.
29. Wernimont, A. K., Huffman, D. L., Lamb, A. L., O'Halloran, T. V., and Rosenzweig, A. C. (2000) Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins, Nat. Struct. Biol. 7, 766-771.
30. Walker, J. M., Tsivkovskii, R., and Lutsenko, S. (2002) Metallochaperone Atox1 transfers copper to the NH2-terminal domain of the Wilson's disease protein and regulates its catalytic activity, J. Biol. Chem. 277, 27953-27959.
31. Voskoboinik, I., Strausak, D., Greenough, M., Brooks, H., Petris, M., Smith, S., Mercer, J. F., and Camakaris, J. (1999) Functional analysis of the N-terminal CXXC metal-binding motifs in the human Menkes copper-transporting P-type ATPase expressed in cultured mammalian cells, J. Biol. Chem. 274, 22008-22012.
32. Fan, B., and Rosen, B. P. (2002) Biochemical characterization of CopA, the Escherichia coli Cu(I)-translocating P-type ATPase, J. Biol. Chem. 277, 46987-46992.
33. +-ATPase CopA, Biochemistry 42, 11040-11047.
34. 2+-ATPase: Functional role of its histidine-rich N-terminal metal binding domain, J. Biol. Chem. 278, 40534-40541.
35. Tsivkovskii, R., MacArthurs, B., and Lutsenko, S. (2001) The Lys(1010)-Lys(1325) fragment of the Wilson's disease protein binds nucleotides and interacts with the N-terminal domain of this protein in a copper-dependent manner, J. Biol. Chem. 276, 2234-2242.
36. Petris, M. J., Mercer, J. F., Culvenor, J. G., Lockhart, P., Gleeson, P. A., and Camakaris, J. (1996) Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking, EMBO J. 15, 6084-6095.
37. Schaefer, M., Hopkins, R. G., Failla, M. L., and Gitlin, J. D. (1999) Hepatocyte-specific localization and copper-dependent trafficking of the Wilson's disease protein in the liver, Am. J. Physiol. 276, G639-G646.
38. 1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels, FEBS Lett. 579, 783-791.
39. Banci, L., Bertini, I., Ciofi-Baffoni, S., Su, X.-C., Miras, R., Bal, N., Mintz, E., Catty, P., Shokes, J. E., and Scott, R. A. (2006) Structural basis for metal binding specificity: the N-terminal cadmium binding domain of the P1-type ATPase CadA, J. Mol. Biol. 356, 638-650.
40. Banci, L., Bertini, I., Ciofi-Baffoni, S., Finney, L. A., Outten, C. E., and O'Halloran, T. V. (2002) A new Zinc-protein coordination site in intracellular metal trafficking: solution structure of the apo and Zn(II) forms of ZntA (46-118), J. Mol. Biol. 323, 883-897.
41. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
42. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
43. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate, Anal. Biochem. 100, 95-97.
44. Liu, J., Stemmler, A. J., Fatima, J., and Mitra, B. (2005) Metal-binding characteristics of the amino-terminal domain of ZntA: binding of lead is different compared to cadmium and zinc, Biochemistry 44, 5159-5167.
45. Guo, J., and Giedroc, D. P. (1997) Zinc site redesign in T4 gene 32 protein: structure and stability of Co(II) complexes formed by wild-type and metal ligand substitution mutants, Biochemistry 36, 730-742.
46. Lobley, A., Whitmore, L., and Wallace, B. A. (2002) DICHROWEB: an intreactive website for the analysis of protein secondary structure from circular dichroism spectra, Bioinformatics 18, 211-212.
47. Whitmore, L., and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data, Nucleic Acids Res. 32, W668-W673.
48. Andrade, M. A., Chacón, P., Merelo, J. J., and Morán, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism using an unsupervised learning neural network, Protein Eng. 6, 383-390.
49. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22, 4673-4680.
50. Page, R. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers, Appl. Biosci. 12, 357-358.
51. Pearson, W. R. (1990) Rapid and sensitive sequence comparison with FASTAP and FASTA, Methods Enzymol. 183, 63-98.
52. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modelling, Electrophoresis 18, 2714-2723.
53. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISS-MODEL: an automated protein homology-modeling server, Nucleic Acids Res. 31, 3381-3385.
54. Vriend, G. (1990) WHAT IF: A molecular modelling and drug design program, J. Mol. Graphics 8, 52-56.
55. Hooft, R., Sander, C., Vriend, G., and Abola, E. (1996) Errors in protein structures, Nature 381, 272.
56. Mandal, A. K., Cheung, W. D., and Argüello, J. M. (2002) Characterization of a thermophilic P-type Ag+/Cu+-ATPase from the extremophile Archaeoglobus fulgidus, J. Biol. Chem. 277, 7201-7208.
57. Walkup, G. K., and Imperiali, B. (1997) Fluorescent chemosensors for divalent zinc based on zinc finger domains. Enhanced oxidative stability, metal binding affinity, and structural and functional characterization, J. Am. Chem. Soc. 119, 3443-3450.
58. 2+-ATPase, FEBS Lett. 506, 249-252.
59. Mitra, B., and Sharma, R. (2001) The cysteine-rich amino-terminal domain of ZntA, a Pb(II)/Zn(II)/Cd(II)-translocating ATPase from Escherichia coli, is not essential for its function, Biochemistry 40, 7694-7699.
60. +-cysteinates in the N-terminal domain, J. Biol. Chem. 278, 23163-23170.
61. Anastassopoulou, I., Banci, L., Bertini, I., Cantini, F., Katsari, E., and Rosato, A. (2004) Solution structure of the apo and copper(I)-loaded human metallochaperone HAH1, Biochemistry 43, 13046-13053.
62. 2-terminal domain of the Wilson disease copper-transporting ATPase: implications for in vivo metal ion-mediated regulation of ATPase activity, J. Biol. Chem. 277, 13409-13414.
63. Xiao, Z., Loughlin, F., George, G. N., Howlett, G. J., and Wedd, A. G. (2004) C-terminal domain of the membrane copper transporter Ctr1 from Saccharomyces cerevisiae binds four Cu(I) as a cuprous-thiolate polynuclear cluster: sub-femtomolar Cu(I) affinity of three proteins involved in copper trafficking, J. Am. Chem. Soc. 126, 3081-3090.
64. Urvoas, A., Moutiez, M., Estienne, C., Couprie, J., Mintz, E., and Le Clainche, L. (2004) Metal-binding stoichiometry and selectivity of the copper chaperone CopZ from Enterococcus hirae, Eur. J. Biochem. 271, 993-1003.
65. DeSilva, T. M., Veglia, G., and Opella, S. J. (2005) Solution structures of the reduced and Cu(I) bound forms of the first metal binding sequence of ATP7A associated with Menkes disease, Proteins 61, 1038-1049.
66. Jensen, P. Y., Bonander, N., Máller, L. B., and Farver, O. (1999) Cooperative binding of copper(I) to the metal binding domains in Menkes disease protein, Biochim. Biophys. Acta 1434, 103-113.
67. Voskoboinik, I., Mar, J., Strausak, D., and Camakaris, J. (2001) The regulation of catalytic activity of the Menkes copper-translocating P-type ATPase: Role of high affinity copper-binding sites, J. Biol. Chem. 276, 28620-28627.